Holothurian (Echinodermata) Diversity of the Glorieuses

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Short Communication

Holothurian (Echinodermata) Diversity in the Glorieuses Archipelago (Eparses Islands, France, Mozambique Channel)

Conand Chantal1,2, Thierry Mulochau3 and Chabanet Pascale4 1Laboratoire Ecologie Marine, Université de La Réunion, 97715 Saint Denis, La Réunion, France; 2Muséum Histoire Naturelle, 43 rue Cuvier, 75005 Paris, France; 3Aquarium de La Réunion, Port de plaisance, 97434 Saint-Gilles les Bains, France;4IRD, BP 50172, 97492 Ste Clotilde, La Réunion, France.

Keywords: Holothuria, Glorieuses Islands, Western Indian Ocean, occurrence, diversity, coral reefs

Abstract—Due to their isolation, Eparses Islands provide a valuable opportunity to investigate biodiversity in the absence of anthropogenic infuence. The Glorieuses Archipelago forms part of the Eparses Islands, or the French scattered islands in the Mozambique Channel (Western Indian Ocean). Inventories of several taxa, including the holothurians (Echinodermata), were carried out in December 2012 as part of the BIORECIE (Biodiversity, Resources and Conservation of Eparses Islands) programme. Specimens were collected and photographed on the reef slopes of the island at ten sites down to 20 m and the reef fats at twelve sites. Given the worldwide overexploitation of holothurians, it is important to know their present diversity and distribution in such remote areas. The Holothuria comprised 20 species: 10 species were collected on the slopes and 15 on the reef fats. Despite the limited number of sites surveyed, the occurrence of the different species allowed their categorisation as common, uncommon or rare. The commercial species, Holothuria nobilis, Bohadschia atra and B. subrubra, were common. Comparisons at local and regional scales using the same methodology showed that holothurian diversity in Glorieuses is high, but already occurring illegal fsheries are a serious concern.

INTRODUCTION Since they are remote and have no permanent human population, the Eparses Islands Coral reefs are among the most diverse of provide a valuable opportunity to evaluate marine ecosystems with the highest species coral reef biodiversity without anthropogenic diversity on the globe (Paulay, 1997; Bellwood infuence. Furthermore, the Glorieuses & Hughes, 2001). Numerous reports on their Archipelago, part of the Eparses Islands, was condition over the last decades warn of their declared a Marine Protected Area (MPA) in growing degradation (e.g. Wilkinson, 2004), 2011 and is in need of a management plan owing to increasing anthropogenic pressure. based on scientifc knowledge. To date, knowledge on the Eparses Islands remains

Corresponding author: CC Email:[email protected] 72 C. Chantal et al.

scarce because of their limited accessibility. fats of the Glorieuses have been published The programme BIORECIE (Biodiversity, by Vergonzannes (1977) and, more recently, Resources and Conservation of the Eparses on several sites located on outer reef slope Islands) was devised to inventorise several and reef fat by Mulochau et al. (2008). The taxonomic groups (scleractinians, hydroids, commercial value of the different species algae, echinoderms (including holothurians), varies and the product can be classifed as of crustaceans and fsh) and, more widely, high value, comprising large species such as to survey the health of the coral reefs to the teatfsh Holothuria nobilis, H. fuscogilva identify priority zones for conservation. The and Thelenota ananas; medium value - several Archipelago is composed of two principal Actinopyga, Bohadschia and Stichopus islands, Grande Glorieuses, which is 3 km species; and low value - many smaller species in diameter and characterized by a group of which are harvested when the larger ones have dunes attaining an altitude of 12 m, and Lys been overfshed (Conand, 2004; Purcell et al., Island, or Petite Glorieuse, with a diameter of 2012; Eriksson & Byrne, 2013). The objective 0.6 km and a bog at its centre. Two rip-raps, of this study was to provide an inventory of les Roches Vertes and l'Ile aux Crabes, with the holothurian diversity, compare it with associated sandbars that emerge at low tide, earlier data and estimate the importance of the complete the archipelago, with a land surface Holothuria in the context of poaching on the of 5 km2 and coral reef with an area of 196 Eparses Islands. km2 (Andrefouët et al., 2009). Holothurians are presently overexploited MATERIALS and METHODS worldwide for export of the dried product Bêche-de-mer (or trepang) consumed by Study areas Asiatic populations (Conand 2004, 2006; A multidisciplinary team explored the reef Toral-Granda et al., 2008; Purcell et al., fats of the island at low tide and the reef 2013). The holothurian fsheries in the slopes down to 20 meters using SCUBA in Indian Ocean have been described (Conand, December 2012. Twelve reef fat sites (19, 22, 2008) and their poor management has been 23, 27 to 33, 36, 37) and ten reef slopes (GLO pointed out (Conand & Muthiga, 2007; FAO, 1, 2, 3, 5, 6, 7 and sites 16, 17, 18, 20) were 2013; Muthiga & Conand, 2014). Previous surveyed; details of their locations and depth observations on the holothurians on the reef are presented in Figure 1.

Table 1. Holothurians recorded at ten sites on the reef slopes of the Glorieuses Islands. Family Species Occurrence Holothuriidae Bohadschia atra 1 Holothuriidae Holothuria arenicola 0.10 Holothuriidae Holothuria atra 0.20 Holothuriidae Holothuria hilla 0.10 Holothuriidae Holothuria nobilis 0.30 Holothuriidae Holothuria pardalis 0.20 Holothuriidae Holothuria sp. juv 0.10 Holothuriidae Pearsonothuria graeffei 0.20 Stichopodidae Thelenota ananas 0.20 Chiridotidae Chiridota stuhlmani 0.10 Holothurians of the Glorieuses Archipelago, Western Indian Ocean 73

Figure 1. Map of the Glorieuses Islands in the Mozambique Channel with the sampling sites surveyed in 2012.

Holothurian specimens were collected and RESULTS photographed for identifcation. A preliminary sort of morphs and species was done in the Species lists are presented for the outer feld and the samples were preserved in reef slopes (Table 1) and reef fat habitats 95% ethanol. Identifcation to species level (Table 2). Eight species of the Holothuriidae was undertaken at the Paris MNHN by were observed on the reef slopes (Table 1). morphological and spicule examination. The Bohadschia atra occurred at all sites while taxonomy here follows the World Register the second most frequent species, the teatfsh of Marine Species (Appeltans et al., 2012). Holothuria nobilis, was only observed at three Holothurian occurrence was calculated sites. One juvenile could not be identifed to separately as the number of sites where a species level. Thelenota ananas was the only species was present in the main habitats, member of the Stichopodidae. Chiridota divided by the total number of sites for each stuhlmani, a small species of the Chiridotidae, habitat, and categorized the feld observations was only found at one site. as common, uncommon or rare. Historical On the reef fats, 11 species of surveys (Vergonzannes, 1977; Mulochau et Holothuriidae were observed, the occurrence al., 2008) were used for temporal comparison. of B. atra and H. nobilis respectively 74 C. Chantal et al.

Table 2. Holothurians recorded at twelve sites on the reef fats of the Glorieuses Islands.

Family Species Occurrence Holothuriidae Actinopyga mauritiana 0.25 Holothuriidae Bohadschia atra 0.42 Holothuriidae Bohadschia koellikeri 0.08 Holothuriidae Bohadschia subrubra 0.33 Holothuriidae Holothuria nobilis 0.58 Holothuriidae Holothuria arenicola 0.08 Holothuriidae Holothuria diffcilis 0.08 Holothuriidae Holothuria fuscocinerea 0.33 Holothuriidae Holothuria hilla 0.17 Holothuriidae Holothuria lineata 0.08 Holothuriidae Holothuria pardalis 0.25 Stichopodidae Stichopus chloronotus 0.08 Sclerodactylidae Afrocucumis africana 0.08 Synaptidae Euapta godeffroyi 0.08 Synaptidae Synapta maculata 0.17

comprising 42% and 58% (Table 2) of the author recorded ten species, only H. pardalis population. The Stichopodidae were only being common; it was found again in 2008 represented by S. chloronotus, and the and in the present study. H. arenicola and L. Sclerodactylidae by Afrocucumis africana, semperianum were less common according to found under rubble blocks. The Synaptidae Vegonzannes (1977) and were not recorded in Euapta godeffroyi and Synapta maculata 2008 or 2012. However, this could originate were also observed but not common. from recent taxonomic changes giving rise to species complexes (Conand et al., 2010). DISCUSSION Moreover, Vergonzannes’ (1977) study was limited to reef fats which may explain why We found a total of 20 holothurian species none of the large commercial species (H. during the 2012 BIORECIE survey of the nobilis, large Bohadschia and Thelenota spp) Glorieuses Islands, comprising 15 species on were recorded in 1977, since the dead coral the reef fats and 10 species on the reef slopes. blocks found on the reef fats are not suitable The most common species on the reef fats habitats for these species. More recently, were Holothuria nobilis, Bohadschia atra, Mulochau and Conand (2008) also recorded B. subrubra, H. fuscocinerea and Actinopyga ten species on the Glorieuses reef fats, the mauritiana, and, on the reef slopes, B. atra and most frequent being H. nobilis and Synapta H. nobilis. These species are commercially maculata, and on the reef slopes, B. subrubra valuable, with medium to high values and H. nobilis. Holothuria impatiens and (Conand, 2008; Purcell et al., 2012). Labidodemas rugosum were not collected Previous observations from 1977 and again in 2012. A few photographs of 2008 were used to assess temporal changes holothurians were taken during a three-day in the holothurian species diversity (Table cruise of the Marion Dufresnes at Glorieuses 3). The frst surveys of the reef fats were (2011), showing B. atra, H. fuscogilva, H. undertaken by Vergonzannes (1977). This nobilis, T. ananas, Pearsonothuria graeffei. Holothurians of the Glorieuses Archipelago, Western Indian Ocean 75

Table 3.Holothuroidea found at Glorieuses in the present and previous (Vergonzannes, 1977; Mulochau & Conand, 2008) surveys, and at Europa in 2011 (Conand et al., 2013). Glorieuses Glorieuses Glorieuses Glorieuses Commercial 2012 2008 1977 2011 value Actinopyga mauritiana x Medium Bohadschia atra x x x Medium Bohadschia koellikeri x Low Bohadschia subrubra x x x Medium Holothuria arenicola x x Holothuria atra x x Low Holothuria diffcilis x Holothuria fuscocinerea x Holothuria hilla x x x Holothuria nobilis x x High Holothuria lineata x x Holothuria pardalis x x x Holothuria sp. juv. x Pearsonothuria graeffei x Low Stichopus chloronotus x x Low Thelenota ananas x x High Afrocucumis africana x Euapta godeffroyi x x Synapta maculata x x Chiridota stuhlmani x Holothuria impatiens x x x Labidodemas rugosum x x Holothuria rigida x Holothuria maculosa x Bohadschia marmorata? x Low Labidodemas semperianum x Bohadschia vitiensis x Low Patinapta sp. x

The same survey methods were used Comparisons with other localities in the during the BIORECIE cruise to Europa WIO include the Comoros by Samyn et al. Island in 2011, at the southern end of the (2006) who presented a very detailed and Mozambique Channel (Conand et al,. illustrated study of 40 species, and Mayotte 2013). The holothurians at this island were where Pouget (2005) and Eriksson et al. less diverse than at Glorieuses, comprising (2012) identifed 22 species, many being of only nine species, including the commonly commercial value. Ecological assessments abundant S. chloronotus and the common B. obtained during a WIOMSA/MASMA atra and B. subrubra (Table 3). project (Conand & Muthiga, 2007; Muthiga 76 C. Chantal et al.

& Conand, 2014) have provided updates of Marines Protégées (AAMP) and the Veolia species inventories in Kenya (44 species), Environment Foundation. Our warm thanks Reunion (37 species; see also Conand et al., to J. Poupin for preparing Figure 1. 2010), Madagascar (125), Mozambique, the Tanzanian mainland and Zanzibar (26 species; see also Eriksson et al., 2010), as References well as abundances of the main species. Despite the apparent present abundance of Andréfouet S, Chagnaud N, Kranenburg CJ commercial species at Glorieuses, the question (2009) Atlas of Western Indian Ocean of the illegal fshery of holothurians must be coral reefs. Centre IRD-Nouméa, considered. It did not seem to occur prior to Nouvelle-Calédonie, 157 pp 2012, given previous observations of the high Appeltans W, Bouchet P, Boxshall GA, De value species, but concern is now raised since Broyer C, de Voogd NJ, Gordon DP, seizures within the Exclusive Economic Zone Hoeksema BW, Horton T, Kennedy (EEZ) in 2013 and, very recently in March M, Mees J, Poore GCB, Read G, 2014, when foreign vessels were arrested by Stöhr S, Walter TC, Costello MJ (eds) the French authorities with diving gear and (2012) World Register of Marine one tonne of holothurians preserved in salt Species. (Available at: http://www. (Journal de l’île de La Réunion, 2013; TAAF marinespecies.org) 2014). In the 2012 BIORECIE survey, the white teatfsh H. fuscogilva was not found Bellwood DR, Hughes TP (2001) Regional- again. This may be attributable to poaching of scale assembly rules and biodiversity of this valuable species. coral reefs. Science 292: 1532-1534 This stresses the need for better Conand C (2004) Present status of world sea monitoring and protection of these resources cucumber resources and utilisation, an within the Glorieuses MPA in the Eparses international overview: In: Lovatelli A, Islands. Illegal catches (quantities and species Conand C, Purcell S, Uthicke S, Hamel specifc records) should be documented JF, Mercier A (eds). Advances in sea by the authorities and compared with cucumber aquaculture and management. species abundance in the natural habitat FAO Fisheries Technical Paper (463), by monitoring. Additional sampling in the pp 13-23 Eparses Islands is needed to properly compare the coral reef fauna between the islands over Conand C (2006) Harvest and trade: time, including the commercial holothurian Utilization of sea cucumbers; species, especially in the Mozambique sea cucumber fsheries; current channel, to conserve and protect the resources international trade; illegal, unreported of these remote and relatively pristine areas. and unregulated trade; by-catch; socio- economic characteristics of the trade Acknowledgements–Support for these in sea cucumbers: In Bruckner AW surveys by the TAAF (Terres Australes et (ed) The Proceedings of the CITES Antarctiques Françaises, the 'Forces Armées workshop on the conservation of sea de la Zone Sud de l’Océan Indien' (FAZSOI) cucumbers in the families Holothuriidae is gratefully acknowledged. Financial support and Stichopodidae. NOAA Technical was provided by the Institut Ecologie et Memorandum NMFS-OPR-34, USA, Environnement du Centre National pour pp 51-73 la Recherche (INEE-CNRS), the Institut National des Sciences de l’Univers (INSU), the Conand C, Muthiga N (2007) Commercial sea Institut de Recherche pour le Développement cucumbers: A review for the Western (IRD), the Fondation pour la Recherche sur Indian Ocean. WIOMSA Book Series la Biodiversité (FRB), the Agence des Aires No. 5, 66 pp Holothurians of the Glorieuses Archipelago, Western Indian Ocean 77

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